Application of Large-Scale Parentage Analysis for Investigating Natal Dispersal in Highly Vagile Vertebrates: A Case Study of American Black Bears (\u3ci\u3eUrsus americanus\u3c/i\u3e)

Understanding the factors that affect dispersal is a fundamental question in ecology and conservation biology, particularly as populations are faced with increasing anthropogenic impacts. Here we collected georeferenced genetic samples (n=2,540) from three generations of black bears (Ursus americanus) harvested in a large (47,739 km2), geographically isolated population and used parentage analysis to identify mother-offspring dyads (n=337). We quantified the effects of sex, age, habitat type and suitability, and local harvest density at the natal and settlement sites on the probability of natal dispersal, and on dispersal distances. Dispersal was male-biased (76% of males dispersed) but a small proportion (21%) of females also dispersed, and female dispersal distances (mean ± SE = 48.9±7.7 km) were comparable to male dispersal distances (59.0±3.2 km). Dispersal probabilities and dispersal distances were greatest for bears in areas with high habitat suitability and low harvest density. The inverse relationship between dispersal and harvest density in black bears suggests that 1) intensive harvest promotes restricted dispersal, or 2) high black bear population density decreases the propensity to disperse. Multigenerational genetic data collected over large landscape scales can be a powerful means of characterizing dispersal patterns and causal associations with demographic and landscape features in wild populations of elusive and wide-ranging species

The conservation genetics juggling act: integrating genetics and ecology, science and policy

The field of conservation genetics, when properly implemented, is a constant juggling act integrating molecular genetics, ecology, and demography with applied aspects concerning managing declining species or implementing conservation laws and policies. This young field has grown substantially since the 1980s following the development of polymerase chain reaction and now into the genomics era. Our laboratory has ‘grown up’ with the field, having worked on these issues for over three decades. Our multidisciplinary approach entails understanding the behavior and ecology of species as well as the underlying processes that contribute to genetic viability. Taking this holistic approach provides a comprehensive understanding of factors that influence species persistence and evolutionary potential while considering annual challenges that occur throughout their life cycle. As a federal laboratory, we are often addressing the needs of the U.S. Fish and Wildlife Service in their efforts to list, de-list, or recover species. Nevertheless, there remains an overall communication gap between research geneticists and biologists who are charged with implementing their results. Therefore, we outline the need for a National Center for Small Population Biology to ameliorate this problem and provide organizations charged with making status decisions firmer ground from which to make their critical decisions.Keywords: conservation genetics, annual cycle, inbreeding, migratory connectivity, pedigree analyses, endangered species, effective population size, cross-seasonal interaction

Phylogeography and population structure of least terns (Sterna antillarum)

Historically, least terns (Sterna antillarum) were one of the most common tern species in North America. However, population declines have resulted from direct and indirect anthropogenic pressures on their breeding and foraging habitat. Three subspecies of least terns have been described within the United States: California least tern (S. a. browni), Interior least tern (S. a. athalassos), and East Coast least tern (S. a. antillarum). California and Interior subspecies are listed as endangered under the U.S. Endangered Species Act. However, the taxonomic status of least terns is a highly contentious issue which has implications for setting conservation priorities at erroneous levels of taxonomic distinctness. Thus, understanding population structure and taxonomy is critical for successful conservation of least terns. To clarify the phylogeographic patterns and population structure and evaluate the traditional subspecific designations, we examined variation in two mitochondrial DNA (mtDNA) genes and 10 microsatellite loci among least terns in North America. MtDNA control region sequences and 10 polymorphic microsatellite loci were used to evaluate traditional subspecific designations and genetic structure in least terns. While highly variable, results from mtDNA control region sequences and microsatellite loci did not support the three traditional subspecies that occur in the United States. However, mtDNA pairwise θST comparisons and AMOVA analyses indicated some genetic structure between the California and the remaining Interior/East Coast breeding areas indicating restriction to female-mediated gene flow. We evaluated phylogeographic patterns and demographic history of least terns using the mtDNA NADH dehydrogenase subunit 6 (ND6) sequences. Phylogeographic analysis revealed no association with geography or traditional subspecies designations. Population genetic analysis did reveal slight genetic differentiation between the California breeding areas and all other Interior/East Coast breeding areas. ND6 data indicate least terns have undergone a recent population expansion. Temporal comparisons between four contemporary breeding areas and their historical counterparts found significant difference in nucleotide diversity and seven historical haplotypes were absent from contemporary breeding areas suggesting loss of genetic diversity. This study is the most comprehensive evaluation of the genetic status of least terns, or any tern species, to date. It points to the need for better information on breeding site fidelity and natal philopatry across the species range was well as population-specific movements throughout the annual cycle. These finding should provide a helpful perspective to those planning conservation efforts throughout the species range

Subspecific Status and Population Genetic Structure of Least Terns (\u3ci\u3eSternula antillarum\u3c/i\u3e) Inferred by Mitochondrial DNA Control-Region Sequences and Microsatellite DNA

The taxonomic identity of endangered populations of the Least Tern (Sternula antillarum) has long been debated. Their current conservation status provides even more impetus to examine the taxonomic distinctness of these groups. We used rapidly evolving mitochondrial DNA control-region sequences (840 base pairs; n = 188) and microsatellite DNA data (7 loci; n = 417) to examine genetic structure within and among three subspecies that occur within the United States: California Least Tern (S. a. browni), Interior Least Tern (S. a. athalassos), and Eastern Least Tern (S. a. antillarum). Although significant genetic structure was observed among breeding populations from across the species’ range, our data indicated little evidence of genetic structure within traditional subspecific groups. Isolation-by-distance analyses, however, identified subtle patterns that may reflect sex-specific differences in dispersal behavior. Our analyses likewise demonstrated little population subdivision among subspecific groups, which raises questions regarding the taxonomic status of traditionally defined subspecies. Our findings can therefore be used to consider a reevaluation of Least Tern subspecies by the American Ornithologists’ Union’s Committee on Taxonomy and Nomenclature. We further emphasize the need for studies of range-wide breeding-site fidelity and natal philopatry to better understand interpopulation movements of individuals throughout the annual cycle

Range-wide Phylogeographic Analysis of the Spotted Frog Complex (\u3ci\u3eRana luteiventris\u3c/i\u3e and \u3ci\u3eRana pretiosa\u3c/i\u3e) in Northwestern North America

The dynamic geological and climatic history of northwestern North America has made it a focal region for phylogeography. We conducted a range-wide phylogeographic analysis of the spotted frog complex (Rana luteiventris and Rana pretiosa) across its range in northwestern North America to understand its evolutionary history and the distribution of clades to inform conservation of R. pretiosa and Great Basin R. luteiventris, candidates for listing under the US Endangered Species Act. Mitochondrial DNA sequence data from a segment of the cytochrome b gene were obtained from 308 R. luteiventris and R. pretiosa from 96 sites. Phylogenetic analysis revealed one main R. pretiosa clade and three main R. luteiventris clades, two of which overlapped in southeastern Oregon. The three R. luteiventris clades were separated from each other by high levels of sequence divergence (average of 4.75–4.97%). Two divergent clades were also uncovered within the Great Basin. Low genetic variation in R. pretiosa and the southeastern Oregon clade of R. luteiventris suggests concern about their vulnerability to extinction

Application of Large-Scale Parentage Analysis for Investigating Natal Dispersal in Highly Vagile Vertebrates: A Case Study of American Black Bears (<i>Ursus americanus</i>)

<div><p>Understanding the factors that affect dispersal is a fundamental question in ecology and conservation biology, particularly as populations are faced with increasing anthropogenic impacts. Here we collected georeferenced genetic samples (n = 2,540) from three generations of black bears (<i>Ursus americanus</i>) harvested in a large (47,739 km²), geographically isolated population and used parentage analysis to identify mother-offspring dyads (n = 337). We quantified the effects of sex, age, habitat type and suitability, and local harvest density at the natal and settlement sites on the probability of natal dispersal, and on dispersal distances. Dispersal was male-biased (76% of males dispersed) but a small proportion (21%) of females also dispersed, and female dispersal distances (mean ± SE  =  48.9±7.7 km) were comparable to male dispersal distances (59.0±3.2 km). Dispersal probabilities and dispersal distances were greatest for bears in areas with high habitat suitability and low harvest density. The inverse relationship between dispersal and harvest density in black bears suggests that 1) intensive harvest promotes restricted dispersal, or 2) high black bear population density decreases the propensity to disperse. Multigenerational genetic data collected over large landscape scales can be a powerful means of characterizing dispersal patterns and causal associations with demographic and landscape features in wild populations of elusive and wide-ranging species.</p></div

Summary of pairwise Euclidean distances for black bear mother-offspring dyads, by offspring sex, including samples sizes (N), and ages of offspring (at time of death), and mothers (at time of offspring birth).

<p>(Dispersers are defined by distances between natal and harvest locations (>30 km for males, and >20 km for females) based on results of an independent genetic spatial autocorrelation analysis)</p

Dispersal probabilities, by age.

<p>Proportion of male (black bars) and female (grey bars) black bears that dispersed, by age. Sample sizes are presented above bars.</p

Distribution of black bear dispersal distances.

<p>Frequency histogram of pairwise distances between black bear mother and offspring dyads, for all individual males (black bars, n = 178) and females (grey bars, n = 159). Distances along the x-axis represent the upper bounds for each bin.</p

Example of black bear dispersal patterns.

<p>Example illustrating three cohorts of offspring from one black bear mother, showing patterns of sex-specific distances, and dispersal patterns in relation to harvest density (low  =  white, high  =  black). Offspring are labeled according to sex and year of birth. Square on inset indicates approximate area in Michigan.</p